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Phylogenetic Analyses Reveal the Shady History of C4 Grasses Erika J

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Phylogenetic Analyses Reveal the Shady History of C4 Grasses Erika J Phylogenetic analyses reveal the shady history of C4 grasses Erika J. Edwardsa,1 and Stephen A. Smithb aDepartment of Ecology and Evolutionary Biology, Brown University, Providence, RI 02912; and bNational Evolutionary Synthesis Center, Durham, NC 27705 Edited by Michael J. Donoghue, Yale University, New Haven, CT, and approved December 31, 2009 (received for review August 24, 2009) Grasslands cover more than 20% of the Earth's terrestrial surface, has provided a strong selection pressure for C4 evolution in and their rise to dominance is one of the most dramatic events of eudicots (4). Grasses have long been viewed as an interesting biome evolution in Earth history. Grasses possess two main photo- exception to this pattern (9). Significant positive correlations synthetic pathways: the C3 pathway that is typical of most plants between C4 grass abundance and growing season temperature and a specialized C4 pathway that minimizes photorespiration and have been documented at both continental and regional scales thus increases photosynthetic performance in high-temperature (10–13); C4 grasses dominate tropical grasslands and savannas and/or low-CO2 environments. C4 grasses dominate tropical and but are virtually absent from cool-temperate grasslands and subtropical grasslands and savannas, and C3 grasses dominate the steppes. Furthermore, both experimental measurements of world's cooler temperate grassland regions. This striking pattern photosynthetic light use efficiency (termed “quantum yield”), has been attributed to C4 physiology, with the implication that the and predictions of leaf models of C3 and C4 photosynthesis evolution of the pathway enabled C4 grasses to persist in warmer provide strong evidence that C4 grasses outperform C3 grasses at climates than their C3 relatives. We combined geospatial and higher temperatures (5, 14–16). Most studies concerning C4 molecular sequence data from two public archives to produce a grasses and precipitation have focused on C3/C4 mixed temper- 1,230-taxon phylogeny of the grasses with accompanying climate ate grassland systems, where the timing of C4 growth often is data for all species, extracted from more than 1.1 million herba- restricted to periods with significant rainfall (12, 13, 17, 18). rium specimens. Here we show that grasses are ancestrally a The C4 pathway thus has been largely dismissed as an adap- warm-adapted clade and that C evolution was not correlated 4 tation to water stress in grasses, with all data indicating that C4 with shifts between temperate and tropical biomes. Instead, 18 evolution allowed grasses to invade and diversify successfully of 20 inferred C origins were correlated with marked reductions 4 into hot climates. However, few studies have compared C4 in mean annual precipitation. These changes are consistent with a grasses with their closest living C3 relatives. C4 origins are not shift out of tropical forest environments and into tropical wood- distributed uniformly across Poaceae but are clustered in one land/savanna systems. We conclude that C4 evolution in grasses major grass lineage, informally named the “PACMAD” clade (3, coincided largely with migration out of the understory and into 6). Most of the C3 grasses that dominate cool-climate grasslands open-canopy environments. Furthermore, we argue that the evo- belong to the Pooideae, a lineage that last shared a common lution of cold tolerance in certain C3 lineages is an overlooked ancestor with PACMAD grasses ≈65–50 Mya (19). It thus is fl innovation that has profoundly in uenced the patterning of grass- possible that differences between Pooideae and PACMAD land communities across the globe. grasses that have nothing to do with photosynthetic pathway variation are driving the apparently strong sorting of C3 and C4 C photosynthesis | climate niche evolution | cold tolerance | phylogeny 4 species along temperature gradients. We employed an explicitly phylogenetic approach to assess the “ ” he term C4 photosynthesis refers to a suite of biochemical and evolutionary history of climate niche space for grasses on a fi Tanatomical modi cations to the standard plant C3 photosynthetic worldwide scale. We used two public archives of data to build the fi pathway that work to concentrate CO2 around the carbon- xing most inclusive phylogeny for Poaceae that permitted analysis of a enzyme Rubisco. The C4 pathway greatly improves photosynthetic climate dataset for all taxa (Materials and Methods). This analysis performance in situations that promote photorespiration, typically resulted in a 1,230 taxon tree with broad coverage of all of the high-temperature and low-CO2 environments (1). The pathway also major Poaceae lineages and, importantly, good sampling of fi promotes more ef cient photosynthetic water use, because the CO2 known C3 and C4 transitions. Our phylogenetic tree includes concentration mechanism allows C4 plants to maintain a lower sto- roughly 10% of all Poaceae species and is the largest grass matal conductance for a given photosynthetic rate. C4 photosynthesis is phylogeny built to date. We identified 21 nodes representing estimatedtohaveevolvedatleast50timesinterrestrialplants(2,3)and evolutionary transitions between photosynthetic types and used ∼ is most prominent in grasses, where roughly half the species ( 5,000) these nodes to generate phylogenetically independent C3/C4 are C4 (4), including economically important species such as maize, pairwise comparisons (Tables S1 and S2) (20). Nearly all iden- sugarcane, sorghum, and switchgrass. C4 grasses currently dominate tified photosynthetic transitions were reconstructed as C4 origins, wide regions of the Earth, and it is estimated that they account for up to with one purported reversal. Fifteen of the 21 transitions 25% of global annual terrestrial primary production (5). occurred within the Panicoideae, a major PACMAD lineage Recent studies suggest that C4 photosynthesis is a relatively containing more than 3,000 species. To account for topological recent innovation in plants, with the earliest appearances coin- uncertainty in this area of the phylogeny, we performed Bayesian ciding with plummeting atmospheric CO2 levels during the mid- analyses for a 299-taxon Panicoideae dataset and ran all diver- Oligocene and many origins occurring much later (4, 6). In grasses, the evolutionary history of C4 photosynthesis is complex, with multiple origins, probable reversals, and a general lag-time Author contributions: E.J.E. and S.A.S. designed research, performed research, analyzed between the evolution of the pathway and the formation of C4- data, and wrote the paper. fl dominated ecosystems (3, 6–8). Although low atmospheric CO2 The authors declare no con ict of interest. certainly was a prerequisite for C4 evolution, it is thought that This article is a PNAS Direct Submission. multiple stressors worked in concert to promote the pathway. C4 1To whom correspondence should be addressed. E-mail: [email protected]. plants are notably prevalent in arid, high-light, saline, and dis- This article contains supporting information online at www.pnas.org/cgi/content/full/ turbed environments, and it is largely accepted that water stress 0909672107/DCSupplemental. 2532–2537 | PNAS | February 9, 2010 | vol. 107 | no. 6 www.pnas.org/cgi/doi/10.1073/pnas.0909672107 Downloaded by guest on September 30, 2021 gence analyses across the Bayesian posterior distribution of analysis of the Hawaiian grass flora that used a similar approach trees. We also used this reduced dataset to reconstruct envi- but was based on very limited geographic and phylogenetic ronmental niche evolution in the Panicoideae and tested sampling (21). whether shifts between photosynthetic types corresponded with Analyses of niche evolution within Panicoideae provided fur- significant changes in temperature and precipitation niche ther support that C4 evolution was associated with shifts into optima under a stabilizing selection model of evolution. drier, but not warmer, environments. For most climate variables, two-optimum stabilizing selection Ornstein-Uhlenbeck (OU) Results models were preferred over Brownian motion or single-optimum Climate data extracted from all available geo-referenced her- models, implying that C3 and C4 lineages have experienced barium material provided clear evidence that certain grass line- divergent selection over time (Table 2). However, the mean C3 ages have specialized in certain habitats (Fig. 1). Importantly, and C4 temperature optima were not largely different, and in all two strictly C3 grass lineages, the Pooideae and the Dantho- cases, the model inferred lower temperature optima for C4 nioideae, stood apart as inhabiting much cooler environments, Panicoideae lineages than for C3 Panicoideae lineages. MAP measured either by mean annual temperature (MAT) (Fig. 1) or received the strongest support for a two-optimum model, with temperature of the wettest, coldest, or warmest month (Fig. S1). the C4 optimum inferred to be drier than the C3 optimum by −1 All other C3 lineages were indistinguishable from C4 lineages more than 500 mm year . with respect to their temperature profiles. Distinctive sorting of precipitation variables was less apparent, although Pooideae Discussion occupied the drier end of the spectrum alongside the C4 lineages These analyses provide clear evidence that C4 origins in grasses Aristidoideae and Chloridoideae (Fig. S2). coincided with ecological shifts into drier environments. How- Our phylogenetic analyses concurred with these general tem-
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